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Barson, N. J.

Publications and source records attributed to Barson, N. J..

6 recordsLinked to original sources

PRDM9 Alleles Guide Distinct Patterns of Recombination Localization in Atlantic Salmon

Meiotic recombination in many vertebrate lineages is directed to genomic regions by the DNA-binding protein PRDM9. To date, PRDM9 research has focused primarily on mammals, and its role in recombination localization has only recently been established in salmonids. PRDM9 binding specificity is determined by a tandemly repeated zinc-finger array that exhibits extensive allelic diversity within and between species. However, the extent to which PRDM9 variation shapes recombination landscapes in salmonids remains poorly understood. Here, we performed large-scale genotyping of PRDM9 in an aquaculture population of Atlantic salmon (Salmo salar) using long-read sequencing. By integrating PRDM9 genotypes with pedigree information and genome-wide recombination data, we generated PRDM9-specific linkage maps and sets of inferred crossover events. We show that the presence of specific PRDM9 alleles is associated with differences in recombination localization and identify patterns consistent with dominance interactions between alleles. Using population-averaged recombination rate estimates, we further link a previously described sequence motif enriched in European recombination hotspots to the presence of a common PRDM9 zinc-finger array allele (RPT6a). Together, our results demonstrate functional differences between PRDM9 alleles which contribute to divergence in recombination landscapes in Atlantic salmon, paralleling patterns observed in mammals. The broad geographic distribution of Atlantic salmon, combined with extensive pedigree data generated through aquaculture, highlights its potential as a powerful model for studying PRDM9 function and evolution beyond mammals.

genetics↗

Ancient persistence and recurrent emergence of structural variants across divergent Atlantic salmon lineages

Structural variants (SVs) are a major source of genomic diversity, yet the evolutionary origins of SVs shared across divergent populations remain difficult to resolve. Shared SVs may reflect ancient polymorphism, recurrent mutation, introgression, or subsequent lineage-specific frequency change, but the relative contribution of these processes often remains difficult to distinguish. Here, we investigated SV evolution across four Atlantic salmon (Salmo salar) lineages differing in geography, Europe versus North America, and domestication status, wild versus farmed. Using sensitive SV discovery, stringent genotyping, local PCA, haplotype-distance analyses, and forward simulations, we tested whether broadly shared SVs behave as a single class of variation or separate into distinct evolutionary categories. We generated a high-confidence SV map and found that SVs were enriched in repetitive regions, particularly segmental duplications and LTR retrotransposons, consistent with genome architecture shaping SV formation. Nearly half of high-confidence SVs were shared across all four lineages despite deep continental divergence, and simulations showed that this broad sharing is more consistent with ancient persistence than recurrent mutation alone. In contrast, a small subset of large SVs exhibited complex PCA clustering and multimodal haplotype-distance distributions, consistent with recurrent formation at structurally unstable loci. Large SVs also showed contrasting frequency trajectories between continents, and one immune gene-rich copy-number variable region showed a marked frequency increase in domesticated European salmon. Together, these results show that shared SVs comprise distinct evolutionary categories shaped by ancient persistence, recurrent mutation, and lineage-specific frequency change.

genomics↗

Large-scale eQTL analyses in Atlantic salmon reveal persistent dosage compensation 100 million years after genome duplication.

Whole-genome duplication (WGD) through autopolyploidization has played a role in genome evolution across eukaryotes. A major consequence of WGD is the rewiring of gene regulatory networks, partly driven by selection on dosage balance. In multicellular organisms, evidence for dosage balance selection has relied on comparative patterns of duplicate gene retention and expression, with few studies directly examining regulatory architecture after WGD. Here, we analysed a large-scale eQTL dataset from Atlantic salmon (Salmo salar), which experienced a WGD 100 million years ago. We found that trans-regulatory connections were enriched between duplicated regions, indicating long-term conservation of ancestral interchromosomal regulatory interactions. Overall, 230 duplicated genes (5%) shared eQTLs, suggesting conserved regulatory control. Moreover, 16 gene pairs showed compensatory expression effects mediated by a common regulator, consistent with predictions of the dosage balance hypothesis. These gene pairs were significantly enriched in recently rediploidized regions. Our results indicate long-term maintenance of dosage balance after WGD. TeaserGenetic regulation in Atlantic salmon shows that duplicated genes can remain dosage-balanced across 100 million years of evolution.

evolutionary biology↗

Parallel selection in domesticated Atlantic salmon from divergent founders including parallel selection on WGD-derived homeologous regions

Aquaculture has a considerably shorter history compared to the domestication of plants and animals. Among aquatic species, those that have undergone whole genome duplication events (WGD) seem particularly successful. This suggests that genetic redundancy from WGD is important for domestication, possibly similar to plant domestication. Atlantic salmon (Salmo salar), which has experienced a lineage-specific WGD, has undergone rapid domestication through intensive breeding since the 1960s. Here, we examined the genomic responses to the domestication of Atlantic salmon, including the impacts of WGD, by comparing the whole genome sequence data of aquaculture and wild populations from two lineages: the Eastern and Western Atlantic (Western Norway and North America). Our analysis revealed shared selective sweeps on identical SNPs in major histocompatibility complex (MHC) genes across distinct aquaculture populations compared to their wild counterparts. This SNP level parallelism suggests that a combination of long-term balancing selection and recent human-induced selection has significantly shaped the evolutionary trajectory of MHC genes. In addition, we observed selective sweeps on gene pairs in the homeologous regions originating from WGD, highlighting WGDs role in maintaining genomic variation and potentially reducing pleiotropy through sub-functionalization. This unique type of "parallel" selection contributes to adapting to the intensive artificial conditions of aquaculture. These findings provide valuable insights into the genetic mechanisms of domestication and adaptive responses in Atlantic salmon, suggesting that the salmonid whole genome duplication has underpinned their successful rapid domestication. Our research emphasizes the importance of maintaining genetic diversity to support sustainable aquaculture practices.

genomics↗

Dissecting the loci underlying maturation timing in Atlantic salmon using haplotype and multi-SNP based association methods

Resolving the genetic architecture of fitness-related traits is key to understanding the evolution and maintenance of fitness variation. However, well-characterized genetic architectures of such traits in wild populations remain uncommon. In this study, we used haplotype-based and multi-SNP Bayesian association methods with sequencing data for 313 individuals from wild populations to further characterize known candidate regions for sea age at maturation in Atlantic salmon (Salmo salar). We detected an association at five loci (on chromosomes ssa06, ssa09, ssa21, and ssa25) out of 116 candidates previously identified in an aquaculture strain with maturation timing in wild Atlantic salmon. We found that at each of these five loci, variation explained by the locus was predominantly driven by a single SNP suggesting the genetic architecture of Atlantic salmon maturation includes multiple loci with simple, non-clustered alleles. This highlights the diversity of genetic architectures that can exist for fitness-related traits. Furthermore, this study provides a useful multi-SNP framework for future work using sequencing data to characterize genetic variation underlying phenotypes in wild populations.

evolutionary biology↗

Sex-dependent dominance maintains migration supergene in rainbow trout

Traits with different fitness optima in males and females cause sexual conflict when they have a shared genetic basis. Heteromorphic sex chromosomes can resolve this conflict and protect sexually antagonistic polymorphisms but accumulate deleterious mutations. However, many taxa lack differentiated sex chromosomes, and how sexual conflict is resolved in these species is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 56 Mb double-inversion supergene that mediates sex-specific migration through sex-dependent dominance, a mechanism that reduces sexual conflict. The double-inversion contains key photosensory, circadian rhythm, adiposity, and sexual differentiation genes and displays frequency clines associated with latitude and temperature, revealing environmental dependence. Our results constitute the first example of sex-dependent dominance across a large autosomal supergene, a novel mechanism for sexual conflict resolution capable of protecting polygenic sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutation load of heteromorphic sex chromosomes.

evolutionary biology↗